Aerobic Methanotrophy and Nitrification: Processes and Connections

Abstract

Ammonia and methane are structurally similar molecules. Not surprisingly therefore, microorganisms that use methane as a sole energy source (methanotrophs) and microorganisms that use ammonia as a sole energy source (ammonia oxidisers or nitrifiers) share many similarities. They have several key enzymes in common, most especially the ammonia monooxygenase/particulate methane monooxygenase enzyme family. The two groups are proposed to have a common evolutionary history. They occupy similar ecological niches, and compete for nitrogen. Enzymatically, nitrifiers are capable of methane oxidation, and methanotrophs are capable of nitrification. Microbial ecologists have attempted to find specific inhibitors for either group in order to study their respective roles in the environment. The contribution of ammonia oxidisers to methanotrophy in natural systems appears to be very minor, however methanotrophs may sometimes have important roles in the nitrogen cycle.

Key Concepts:

  • Some bacteria and archaea are capable of using methane or ammonia as energy sources.

  • Methanotrophs and ammonia oxidisers are each highly specialised to living on their particular substrate.

  • Methanotrophs and ammonia oxidisers have several key enzymes in common, and may share a common evolutionary history.

  • Both groups must cope with toxic by‐products of ammonia oxidation.

  • Methanotrophs may be important in the environmental nitrogen cycle, but ammonia oxidisers do not affect the methane cycle.

  • Ammonia oxidising archaea appear to outcompete ammonia oxidising bacteria under ammonia‐limiting and acidic conditions.

Keywords: methane; ammonia; nitrification; methanotrophy; ammonia oxidation; nitrous oxide; denitrification; chemolithotrophy; biogeochemistry

Figure 1.

Overlapping pathways for ammonia and methane oxidation. Black lines denote bacterial pathways; grey lines denote putative pathways for ammonia‐oxidising thaumarchaea. Enzymes catalysing each process are: a, ammonia/methane monooxygenase; b, hydroxylamine oxidoreductase; c, nitrite reductase; d, nitric oxide reductase; e, methanol dehydrogenase; f, formaldehyde dehydrogenase; g, formate dehydrogenase; h, enzymes of the serine or ribulose monophosphate pathway and i, enzymes of the Calvin–Benson–Bassham cycle. The question marks in the thaumarchaeal pathway denote uncertainty regarding the intermediate produced by ammonia monooxygenase, the enzyme that oxidises this intermediate to nitrite, and enzymes that form NO/N2O from the intermediate of ammonia oxidation or from reduction of nitrite as measured by Santoro et al. . The dashed line denotes a possible role of NO in ammonia‐oxidation (Schleper and Nicol, ).

Figure 2.

Phylogenetic tree of partial (495 nucleotides) pmoA/amoA gene sequences of major groups of ammonia oxidisers and methanotrophs. The accession numbers of the sequences used to create the tree are shown. The tree was constructed with TREE_PUZZLE, a quartet maximum‐likelihood method, using a Schoeniger–von Hasseler distance calculation (Schmidt et al., ). Support values for major nodes are given, and multifurcations are drawn when the support for a bifurcation is <50%. The bar represents 0.2 changes per nucleotoide position.

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References

Acton SD and Baggs EM (2011) Interactions between N application rate, CH4 oxidation and N2O production in soil. Biogeochemistry 103: 15–26.

Bédard C and Knowles R (1989) Physiology, biochemistry, and specific inhibitors of CH4, NH4+, and CO oxidation by methanotrophs and nitrifiers. Microbiology and Molecular Biology Reviews 53: 68–84.

Belova SE, Baani M, Suzina NE et al. (2011) Acetate utilization as a survival strategy of peat‐inhabiting Methylocystis spp. Environmental Microbiology Reports 3: 36–46.

Bodelier PLE and Frenzel P (1999) Contribution of methanotrophic and nitrifying bacteria to CH4 and NH4+ oxidation in the rhizosphere of rice plants as determined by new methods of discrimination. Applied and Environmental Microbiology 65: 1826–1833.

Bodelier PLE and Laanbroek HJ (2004) Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiology Ecology 47: 265–277.

Bosse U, Frenzel P and Conrad R (1993) Inhibition of methane oxidation by ammonium in the surface‐layer of a littoral sediment. FEMS Microbiology Ecology 13: 123–134.

Campbell MA, Nyerges G, Kozlowski JA et al. (2011) Model of the molecular basis for hydroxylamine oxidation and nitrous oxide production in methanotrophic bacteria. FEMS Microbiology Letters 322: 82–89.

Canfield DE, Glazer AN and Falkowski PG (2010) The evolution and future of Earth's nitrogen cycle. Science 330: 192–196.

Chistoserdova L, Kalyuzhnaya MG and Lidstrom ME (2009) The expanding world of methylotrophic metabolism. Annual Review of Microbiology 63: 477–499.

Conrad R (2007) Microbial ecology of methanogens and methanotrophs. Advances in Agronomy 96: 1–63.

Dedysh SN, Belova SE, Bodelier PLE et al. (2007) Methylocystis heyeri sp. nov., a novel type II methanotrophic bacterium possessing the ‘signature’ fatty acid of type I methanotrophs. International Journal of Systematic and Evolutionary Microbiology 57: 472–479.

Dedysh SN, Knief C and Dunfield PF (2005) Methylocella species are facultatively methanotrophic. Journal of Bacteriology 187: 4665–4670.

Dunfield PF (2006) The soil methane sink. In: Reay D, Hewitt CN, Smith K and Grace J (eds) Greenhouse Gas Sinks, pp. 152–170. Wallingford, UK: CABI Publishing.

Dunfield PF, Belova SE, Vorob'ev AV et al. (2010) Methylocapsa aurea sp nov., a facultatively methanotrophic bacterium possessing a particulate methane monooxygenase. International Journal of Systematic and Evolutionary Microbiology 60: 2659–2664.

Ettwig KF, Butler MK, Le Paslier D et al. (2010) Nitrite‐driven anaerobic methane oxidation by oxygenic bacteria. Nature 464: 543–548.

Frenzel P and Bosse U (1996) Methyl fluoride, an inhibitor of methane oxidation and methane production. FEMS Microbiology Ecology 21: 25–36.

Hakemian AS and Rosenzweig AC (2007) The biochemistry of methane oxidation. Annual Review of Biochemistry 76: 223–241.

Hanson RS and Hanson TE (1996) Methanotrophic bacteria. Microbiological Reviews 60: 439–471.

Heyer J, Berger U, Hardt M and Dunfield PF (2005) Methylohalobius crimeensis gen. nov., sp. nov., a moderately halophilic, methanotrophic bacterium isolated from hypersaline lakes of Crimea. International Journal of Systematic and Evolutionary Microbiology 55: 1817–1826.

Im J, Lee S‐W, Bodrossy L, Barcelona MJ and Semrau JD (2011) Field application of nitrogen and phenylacetylene to mitigate greenhouse gas emissions from landfill cover soils: effects on microbial community structure. Applied Microbiology and Biotechnology 89: 189–200.

Juliette LY, Hyman MR and Arp DJ (1993) Mechanism‐based inactivation of ammonia monooxygenase in Nitrosomonas europaea by allylsulfide. Applied and Environmental Microbiology 59: 3728–2735.

Khadem AF, Pol A, Wieczorek A et al. (2011) Autotrophic methanotrophy in verrucomicrobia: Methylacidiphilum fumariolicum SolV uses the Calvin–Benson–Bassham Cycle for carbon dioxide fixation. Journal of Bacteriology 193: 4438–4446.

Klotz MG and Stein LY (2008) Nitrifier genomics and evolution of the nitrogen cycle. FEMS Microbiology Letters 278: 146–456.

Könneke M, Bernhard AE, de la Torre JR et al. (2005) Isolation of an autotrophic ammonia‐oxidizing marine archaeon. Nature 437: 543–546.

Laanbroek HJ (2010) Methane emission from natural wetlands: interplay between emergent macrophytes and soil microbial processes. A mini‐review. Annals of Botany 105: 141–153.

Lee SW, Im J, DiSpirito AA et al. (2009) Effect of nutrient and selective inhibitor amendments on methane oxidation, nitrous oxide production, and key gene presence and expression in landfill cover soils: characterization of the role of methanotrophs, nitrifiers, and denitrifiers. Applied Microbiology and Biotechnology 85: 389–403.

Lontoh S, DiSpirito AA, Crema CL et al. (2000) Differential inhibition in vivo of ammonia monooxygenase, soluble methane monooxygenase and membrane‐associated methane monooxygenase by phenylacetylene. Environmental Microbiology 2: 485–494.

Mandernack KW, Kinney CA, Coleman D et al. (2000) The biogeochemical controls of N2O production and emission in landfill cover soils: the role of methanotrophs in the nitrogen cycle. Environmental Microbiology 2: 298–309.

Mandernack KW, Mills CT, Johnson CA et al. (2009) The δ15N and δ18O values of N2O produced during the co‐oxidation of ammonia by methanotrophic bacteria. Chemical Geology 267: 96–107.

Martens‐Habbena W, Berube PM, Urakawa H et al. (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461: 976–979.

Megraw SR and Knowles R (1989) Methane‐dependent nitrate production by a microbial consortium enriched from a cultivated humisol. FEMS Microbiology Ecology 62: 359–366.

Miller LG, Coutlakis MD, Oremland RS et al. (1993) Selective inhibition of ammonium oxidation and nitrification‐linked N2O formation by methyl fluoride and dimethyl ether. Applied and Environmental Microbiology 59: 2457–2464.

Noll M, Frenzel P and Conrad R (2008) Selective stimulation of type I methanotrophs in a rice paddy soil by urea fertilization revealed by RNA‐based stable isotope probing. FEMS Microbiology Ecology 65: 125–132.

Nyerges G, Han SK and Stein LY (2010) Effects of ammonium and nitrite on growth and competitive fitness of cultivated methanotrophic bacteria. Applied and Environmental Microbiology 76: 5648–5651.

Nyerges G and Stein LY (2009) Ammonia co‐metabolism and product inhibition vary considerably among species of methanotrophic bacteria. FEMS Microbiology Letters 297: 131–136.

Offre P, Prosser JI and Nicol GW (2009) Growth of ammonia‐oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiology Ecology 70: 99–108.

Op den Camp HJM, Islam T, Stott MB et al. (2009) Minireview: environmental, genomic, and taxonomic perspectives on methanotrophic Verrucomicrobia. Environmental Microbiology Reports 1: 293–306.

Oremland RS and Culbertson CW (1992) Importance of methane‐oxidizing bacteria in the methane budget as revealed by the use of a specific inhibitor. Nature 356: 421–423.

Roy R and Knowles R (1995) Differential inhibition by allylsulfide of nitrification and methane oxidation in freshwater sediment. Applied and Environmental Microbiology 61: 4278–4283.

Saari A and Martikainen PJ (2001) Differential inhibition of methane oxidation and nitrification in forest soils by dimethyl sulfoxide (DMSO). Soil Biology and Biochemistry 33: 1567–1570.

Santoro AE, Buchwald C, McIlvin MR and Casciotti KL (2011) Isotopic signature of N2O produced by marine ammonia‐oxidizing archaea. Science 333: 1282–1285.

Schleper C and Nicol GW (2010) Ammonia‐oxidising archaea – physiology, ecology and evolution. Advances in Microbial Physiology 57: 1–41.

Schmidt HA, Strimmer K, Vingron M and Haeseler A (2002) TREE‐PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502–504.

Semrau JD, DiSpirito AA and Yoon S (2010) Methanotrophs and copper. FEMS Microbiology Reviews 34: 496–531.

Stein LY (2011) Heterotrophic nitrification and nitrifier denitrification. In: Ward BB, Arp DJ and Klotz MG (eds) Nitrification, pp. 95–114. Washington, DC: ASM Press.

Sutka RL, Ostrom NE, Ostrom PH et al. (2003) Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europeae and Methyloccus capsulatus Bath. Rapid Communication in Mass Spectrometry 17: 738–745.

Tavormina PL, Orphan VJ, Kalyuzhnaya MG et al. (2011) A novel family of functional operons encoding methane/ammonia monooxygenase‐related proteins in gammaproteobacterial methanotrophs. Environmental Microbiology Reports 3: 91–100.

Tourna M, Stieglmeier M, Spang A et al. (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proceedings of the National Academy of Sciences of the USA 108: 8420–8425.

Wrage N, Velthof GL, van Beusichem ML and Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biology and Biochemistry 33: 1723–1732.

Yao H, Gao Y, Nicol GW et al. (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Applied and Environmental Microbiology 77: 4618–4625.

Further Reading

Arp DJ and Stein LY (2003) Metabolism of inorganic N compounds by ammonia‐oxidizing bacteria. Critical Reviews in Biochemistry and Molecular Biology 38: 471–495.

Chistoserdova L, Vorholt JA and Lidstrom ME (2005) A genomic view of methane oxidation by aerobic bacteria and anaerobic archaea. Genome Biology 6: 208.

Dalton H (2005) The Leeuwenhoek Lecture 2000. The natural and unnatural history of methane‐oxidising bacteria. Philosophical Transactions of the Royal Society B 360: 1207–1222.

Dedysh SN and Dunfield PF (2010) Facultative methanotrophs. In: Timmis KN (ed.) Handbook of Hydrocarbon and Lipid Microbiology, pp. 1967–1976. Berlin: Springer‐Verlag.

Jetten MSM, Niftrik L, Strous M et al. (2009) Biochemistry and molecular biology of anammox bacteria. Critical Reviews in Biochemistry and Molecular Biology 44: 65–84.

Klotz MG and Stein LY (eds) (2011) Research on Nitrification and Related Processes, Part B. San Diego, CA: Elsevier.

Rosenzweig A and Ragsdale SW (eds) (2011) Methods in Methane Metabolism, Part B: Methanotrophy. Methods in Enzymology, vol. 495. London: Academic Press.

Scheutz C, Kjeldsen P, Bogner JE et al. (2009) Microbial methane oxidation processes and technologies for mitigation of landfill gas emissions. Waste Management and Research 27: 409–455.

Trotsenko YA and Murrell JC (2008) Metabolic aspects of aerobic obligate methanotrophy. Advances in Applied Microbiology 63: 183–229.

Ward BB, Arp DJ and Klotz MG (eds) (2011) Nitrification. Washington, DC: ASM Press.

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Stein, Lisa Y, Roy, Réal, and Dunfield, Peter F(Apr 2012) Aerobic Methanotrophy and Nitrification: Processes and Connections. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022213]